Galectin-9 functionally impairs natural killer cells in humans and mice

Journal of Virology

Volumn 87, Issue 9, 2013, Pages 4835-4845

  Golden Mason, Lucy ^a,b,c   McMahan, Rachel H ^a,c   Strong, Michael ^d   Reisdorph, Richard ^b,e   Mahaffey, Spencer ^b   Palmer, Brent E ^f   Cheng, Linling ^a   Kulesza, Caroline ^g   Hirashima, Mitsuomi ^h   Niki, Toshiro ^h   Rosen, Hugo R ^a,b,c  

^a UNIVERSITY OF COLORADO   (United States)

^b NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d Environment and Health   (United States)

^e UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^f Division of Allergy and Clinical Immunology   (United States)

^g UCD   (United States)

^h KAGAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; ECALECTIN; GAMMA INTERFERON; T CELL IMMUNOGLOBULIN AND MUCIN DOMAIN CONTAINING MOLECULE 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL COUNT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGRANULATION; FEMALE; HUMAN; HUMAN CELL; LYMPHOCYTE FUNCTION; LYMPHOKINE ACTIVATED KILLER CELL; MICROARRAY ANALYSIS; MOUSE; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; GALECTINS; HERPESVIRIDAE INFECTIONS; HUMANS; INTERLEUKIN-12; INTERLEUKIN-15; KILLER CELLS, NATURAL; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUROMEGALOVIRUS; RECEPTORS, VIRUS;

HEPATITIS C VIRUS; MURID HERPESVIRUS 1; MUS;

EID: 84876320083     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01085-12     Document Type: Article

References (50)

1. Barondes SH, Cooper DN, Gitt MA, Leffler H. 1994. Galectins. Structure and function of a large family of animal lectins. J. Biol. Chem. 269:20807-20810.
2. Wada J, Kanwar YS. 1997. Identification and characterization of galectin-9, a novel beta-galactoside-binding mammalian lectin. J. Biol. Chem. 272:6078-6086.
3. Mengshol JA, Golden-Mason L, Arikawa T, Smith M, Niki T, McWilliams R, Randall JA, McMahan R, Zimmerman MA, Rangachari M, Dobrinskikh E, Busson P, Polyak SJ, Hirashima M, Rosen HR. 2010. A crucial role for Kupffer cell-derived galectin-9 in regulation of T cell immunity in hepatitis C infection. PLoS One 5:e9504. doi:10.1371/journal .pone.0009504.
4. Elahi S, Niki T, Hirashima M, Horton H. 2012. Galectin-9 binding to Tim-3 renders activated human CD4+ T cells less susceptible to HIV-1 infection. Blood 119:4192-4204.
5. Freeman GJ, Casasnovas JM, Umetsu DT, DeKruyff RH. 2010. TIM genes: a family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol. Rev. 235:172-189.
6. Pioche-Durieu C, Keryer C, Souquere S, Bosq J, Faigle W, Loew D, Hirashima M, Nishi N, Middeldorp J, Busson P. 2005. In nasopharyngeal carcinoma cells, Epstein-Barr virus LMP1 interacts with galectin 9 in membrane raft elements resistant to simvastatin. J. Virol. 79:13326-13337.
7. Bi S, Hong PW, Lee B, Baum LG. 2011. Galectin-9 binding to cell surface protein disulfide isomerase regulates the redox environment to enhance Tcell migration andHIVentry. Proc. Natl. Acad. Sci. U. S. A. 108:10650-10655.
8. Rabinovich GA, Toscano MA. 2009. Turning "sweet" on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat. Rev. Immunol. 9:338-352.
9. Wiersma VR, de Bruyn M, Helfrich W, Bremer E. 2011. Therapeutic potential of galectin-9 in human disease. Med. Res. Rev. doi:10.1002/med .20249. [Epub ahead of print.]
10. Dai SY, Nakagawa R, Itoh A, Murakami H, Kashio Y, Abe H, Katoh S, Kontani K, Kihara M, Zhang SL, Hata T, Nakamura T, Yamauchi A, Hirashima M. 2005. Galectin-9 induces maturation of human monocytederived dendritic cells. J. Immunol. 175:2974-2981.
11. Oomizu S, Arikawa T, Niki T, Kadowaki T, Ueno M, Nishi N, Yamauchi A, Hirashima M. 2012. Galectin-9 suppresses Th17 cell development in an IL-2-dependent but Tim-3-independent manner. Clin. Immunol. 143:51-58.
12. Klibi J, Niki T, Riedel A, Pioche-Durieu C, Souquere S, Rubinstein E, Le Moulec S, Guigay J, Hirashima M, Guemira F, Adhikary D, Mautner J, Busson P. 2009. Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood 113:1957-1966.
13. Zhu C, Anderson AC, Schubart A, Xiong H, Imitola J, Khoury SJ, Zheng XX, Strom TB, Kuchroo VK. 2005. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 6:1245-1252.
14. Kadowaki T, Arikawa T, Shinonaga R, Oomizu S, Inagawa H, Soma G, Niki T, Hirashima M. 2012. Galectin-9 signaling prolongs survival in murine lung-cancer by inducing macrophages to differentiate into plasmacytoid dendritic cell-like macrophages. Clin. Immunol. 142:296-307.
15. Seki M, Oomizu S, Sakata KM, Sakata A, Arikawa T, Watanabe K, Ito K, Takeshita K, Niki T, Saita N, Nishi N, Yamauchi A, Katoh S, Matsukawa A, Kuchroo V, Hirashima M. 2008. Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. Clin. Immunol. 127:78-88.
16. Biron CA. 1999. Initial and innate responses to viral infections-pattern setting in immunity or disease. Curr. Opin. Microbiol. 2:374-381.
17. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S. 2011. Innate or adaptive immunity? The example of natural killer cells. Science 331:44-49.
18. Biron CA, Brossay L. 2001. NK cells and NKT cells in innate defense against viral infections. Curr. Opin. Immunol. 13:458-464.
19. Cooper MA, Fehniger TA, Caligiuri MA. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22:633-640.
20. Lanier LL. 2005. NK cell recognition. Annu. Rev. Immunol. 23:225-274.
21. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, Biassoni R, Moretta L. 2001. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 19:197-223.
22. Gleason MK, Lenvik TR, McCullar V, Felices M, O'Brien MS, Cooley SA, Verneris MR, Cichocki F, Holman CJ, Panoskaltsis-Mortari A, Niki T, Hirashima M, Blazar BR, Miller JS. 2012. Tim-3 is an inducible human natural killer cell receptor that enhances interferon gamma production in response to galectin-9. Blood 119:3064-3072.
23. Ndhlovu LC, Lopez-Verges S, Barbour JD, Jones RB, Jha AR, Long BR, Schoeffler EC, Fujita T, Nixon DF, Lanier LL. 2012. Tim-3 marks human natural killer cell maturation and suppresses cell-mediated cytotoxicity. Blood 119:3734-3743.
24. Su EW, Bi S, Kane LP. 2011. Galectin-9 regulates T helper cell function independently of Tim-3. Glycobiology 21:1258-1265.
25. Vaitaitis GM, Wagner DH, Jr. 2012. Galectin-9 controls CD40 signaling through a Tim-3 independent mechanism and redirects the cytokine profile of pathogenic T cells in autoimmunity. PLoS One 7:e38708. doi:10 .1371/journal.pone.0038708.
26. Hartmann J, Tran TV, Kaudeer J, Oberle K, Herrmann J, Quagliano I, Abel T, Cohnen A, Gatterdam V, Jacobs A, Wollscheid B, Tampe R, Watzl C, Diefenbach A, Koch J. 2012. The stalk domain and the glycosylation status of the activating natural killer cell receptor NKp30 are important for ligand binding. J. Biol. Chem. 287:31527-31539.
27. Margraf-Schonfeld S, Bohm C, Watzl C. 2011. Glycosylation affects ligand binding and function of the activating natural killer cell receptor 2B4 (CD244) protein. J. Biol. Chem. 286:24142-24149.
28. Mason LH, Willette-Brown J, Anderson SK, Alvord WG, Klabansky RL, Young HA, Ortaldo JR. 2003. Receptor glycosylation regulates Ly-49 binding to MHC class I. J. Immunol. 171:4235-4242.
29. Huang da W, Sherman BT, Tan Q, Kir J, Liu D, Bryant D, Guo Y, Stephens R, Baseler MW, Lane HC, Lempicki RA. 2007. DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res. 35: W169-W175.
30. Smith MG. 1954. Propagation of salivary gland virus of the mouse in tissue cultures. Proc. Soc. Exp. Biol. Med. 86:435-440.
31. Harvey DM, Levine AJ. 1991. p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes Dev. 5:2375-2385.
32. Wagner M, Jonjic S, Koszinowski UH, Messerle M. 1999. Systematic excision of vector sequences from the BAC-cloned herpesvirus genome during virus reconstitution. J. Virol. 73:7056-7060.
33. Golden-Mason L, Castelblanco N, O'Farrelly C, Rosen HR. 2007. Phenotypic and functional changes of cytotoxic CD56pos natural T cells determine outcome of acute hepatitisCvirus infection. J. Virol. 81:9292-9298.
34. Haybaeck J, Zeller N, Wolf MJ, Weber A, Wagner U, Kurrer MO, Bremer J, Iezzi G, Graf R, Clavien PA, Thimme R, Blum H, Nedospasov SA, Zatloukal K, Ramzan M, Ciesek S, Pietschmann T, Marche PN, Karin M, Kopf M, Browning JL, Aguzzi A, Heikenwalder M. 2009. A lymphotoxindriven pathway to hepatocellular carcinoma. Cancer Cell 16:295-308.
35. Kuttruff S, Koch S, Kelp A, Pawelec G, Rammensee HG, Steinle A. 2009. NKp80 defines and stimulates a reactive subset of CD8 T cells. Blood 113:358-369.
36. Lichtfuss GF, Meehan AC, Cheng WJ, Cameron PU, Lewin SR, Crowe SM, Jaworowski A. 2011. HIV inhibits early signal transduction events triggered by CD16 cross-linking on NK cells, which are important for antibody-dependent cellular cytotoxicity. J. Leukoc. Biol. 89:149-158.
37. Filen JJ, Filen S, Moulder R, Tuomela S, Ahlfors H, West A, Kouvonen P, Kantola S, Bjorkman M, Katajamaa M, Rasool O, Nyman TA, Lahesmaa R. 2009. Quantitative proteomics reveals GIMAP family proteins 1 and 4 to be differentially regulated during human T helper cell differentiation. Mol. Cell. Proteomics 8:32-44.
38. Saunders A, Webb LM, Janas ML, Hutchings A, Pascall J, Carter C, Pugh N, Morgan G, Turner M, Butcher GW. 2010. Putative GTPase GIMAP1 is critical for the development of mature B and T lymphocytes. Blood 115:3249-3257.
39. Khor CC, Vannberg FO, Chapman SJ, Guo H, Wong SH, Walley AJ, Vukcevic D, Rautanen A, Mills TC, Chang KC, Kam KM, Crampin AC, Ngwira B, Leung CC, Tam CM, Chan CY, Sung JJ, Yew WW, Toh KY, Tay SK, Kwiatkowski D, Lienhardt C, Hien TT, Day NP, Peshu N, Marsh K, Maitland K, Scott JA, Williams TN, Berkley JA, Floyd S, Tang NL, Fine PE, Goh DL, Hill AV. 2010. CISH and susceptibility to infectious diseases. N. Engl. J. Med. 362:2092-2101.
40. Ma X, Wang X, Gao X, Wang L, Lu Y, Gao P, Deng W, Yu P, Ma J, Guo J, Cheng H, Zhang C, Shi T, Ma D. 2007. Identification of five human novel genes associated with cell proliferation by cell-based screening from an expressed cDNA ORF library. Life Sci. 81:1141-1151.
41. Vujanovic NL. 2011. Role of TNF superfamily ligands in innate immunity. Immunol. Res. 50:159-174.
42. Sehrawat S, Reddy PB, Rajasagi N, Suryawanshi A, Hirashima M, Rouse BT. 2010. Galectin-9/TIM-3 interaction regulates virus-specific primary and memory CD8 T cell response. PLoS Pathog. 6:e1000882. doi:10.1371 /journal.ppat.1000882.
43. Khademi M, Illes Z, Gielen AW, Marta M, Takazawa N, Baecher-Allan C, Brundin L, Hannerz J, Martin C, Harris RA, Hafler DA, Kuchroo VK, Olsson T, Piehl F, Wallstrom E. 2004. T cell Ig-and mucin-domaincontaining molecule-3 (TIM-3) and TIM-1 molecules are differentially expressed on human Th1 and Th2 cells and in cerebrospinal fluid-derived mononuclear cells in multiple sclerosis. J. Immunol. 172:7169-7176.
44. Smyk-Pearson S, Tester IA, Klarquist J, Palmer BE, Pawlotsky JM, Golden-Mason L, Rosen HR. 2008. Spontaneous recovery in acute human hepatitis C virus infection: functional T-cell thresholds and relative importance of CD4 help. J. Virol. 82:1827-1837.
45. Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T. 2009. Maturation of mouse NK cells is a 4-stage developmental program. Blood 113:5488-5496.
46. Jaeger BN, Donadieu J, Cognet C, Bernat C, Ordonez-Rueda D, Barlogis V, Mahlaoui N, Fenis A, Narni-Mancinelli E, Beaupain B, Bellanne-Chantelot C, Bajenoff M, Malissen B, Malissen M, Vivier E, Ugolini S. 2012. Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J. Exp. Med. 209:565-580.
47. Lassen MG, Lukens JR, Dolina JS, Brown MG, Hahn YS. 2010. Intrahepatic IL-10 maintains NKG2A+Ly49-liver NK cells in a functionally hyporesponsive state. J. Immunol. 184:2693-2701.
48. Mitrovic M, Arapovic J, Traven L, Krmpotic A, Jonjic S. 2012. Innate immunity regulates adaptive immune response: lessons learned from studying the interplay between NK and CD8(+) T cells during MCMV infection. Med. Microbiol. Immunol. 201:487-495.
49. Anderson AC, Anderson DE, Bregoli L, Hastings WD, Kassam N, Lei C, Chandwaskar R, Karman J, Su EW, Hirashima M, Bruce JN, Kane LP, Kuchroo VK, Hafler DA. 2007. Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 318: 1141-1143.
50. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M. 2006. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 34: D354-D357.